Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T07:04:07.834Z Has data issue: false hasContentIssue false

Regulation of seed dormancy and germination by nitrate

Published online by Cambridge University Press:  06 June 2018

Lisza Duermeyer
Affiliation:
Department of Cell and Systems Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario, Canada M5S3B2
Ehsan Khodapanahi
Affiliation:
Department of Cell and Systems Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario, Canada M5S3B2
Dawei Yan
Affiliation:
Department of Cell and Systems Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario, Canada M5S3B2 Department of Plant Sciences, University of California, Davis, CA 95616, USA
Anne Krapp
Affiliation:
Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, 78000, Versailles, France
Steven J. Rothstein
Affiliation:
Department of Molecular and Cellular Biology, University of Guelph, Guelph, Ontario, Canada N1G2W1
Eiji Nambara*
Affiliation:
Department of Cell and Systems Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario, Canada M5S3B2
*
Author for correspondence: Eiji Nambara, Email: eiji.nambara@utoronto.ca

Abstract

Nitrate promotes seed germination at low concentrations in many plant species, and functions as both a nutrient and a signal. As a nutrient, it is assimilated via nitrite to ammonium, which is then incorporated into amino acids. Nitrate reductase (NR) catalyses the reduction of nitrate to nitrite, the committed step in the assimilation. Seed sensitivity to nitrate is affected by other environmental factors, such as light and after-ripening, and by genotypes. Mode of nitrate action in seed germination has been well documented in Arabidopsis thaliana and the hedge mustard Sisymbrium officinale. In these species nitrate promotes seed germination independent of its assimilation by NR, suggesting that it acts as a signal to stimulate germination. In Arabidopsis, maternally applied nitrate affects the degree of primary dormancy in both wild-type and mutants defective in NR. This indicates that nitrate acts not only during germination, but also during seed development to negatively regulate primary dormancy. Functional genomics studies in Arabidopsis have revealed that nitrate elicits downstream events similar to other germination stimulators, such as after-ripening, light and stratification, suggesting that these distinct environmental signals share the same target(s). In Arabidopsis, the NIN-like protein 8 (NLP8) transcription factor, which acts downstream of nitrate signalling, induces nitrate-dependent gene expression. In particular, a gene encoding the abscisic acid (ABA) catabolic enzyme CYP707A2 is directly regulated by NLP8. This regulation triggers a nitrate-induced ABA decrease that permits seed germination. This review article summarizes an update of our current understanding of the regulation of seed dormancy and germination by nitrate.

Type
Review Paper
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albertos, P, Romero-Puertas, M, Tatematsu, K, Mateos, I, Sanchez-Vincente, I, Nambara, E and Lorenzo, O (2015) S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nature Communications 6, 8669.Google Scholar
Alboresi, A, Gestin, C, Leydecker, M-T, Bedu, M, Meyer, C and Truong, H-N (2005) Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant, Cell and Environment 28, 500512.Google Scholar
Ali-Rachedi, S, Bouinot, D, Wagner, M-H, Bonnet, M, Sotta, B, Grappin, P and Jullien, M (2004) Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: studies with the Cape Verde Islands ecotype, the dormant model of Arabidopsis thaliana. Planta 219, 479488.Google Scholar
Arc, E, Chibani, K, Grappin, P, Jullien, M, Godin, B, Cueff, G, Valot, B, Balliau, T, Jon, D and Rajjou, L (2012) Cold stratification and exogenous nitrates entail similar functional proteome adjustments during Arabidopsis seed dormancy release. Journal of Proteome Research 11, 54185432.Google Scholar
Arc, E, Galland, M, Godin, B, Cueff, G and Rajjou, L (2013) Nitric oxide implication in the control of seed dormancy and germination. Frontiers in Plant Science 4, article 346.Google Scholar
Baskin, JM and Baskin, CC (2004) A classification system for seed dormancy. Seed Science Research 14, 116.Google Scholar
Batak, I, Dević, M, Gibal, Z, Grubišić, D, Poff, K. L. and Konjević, R (2002) The effects of potassium nitrate and NO-donors on phytochrome A- and phytochrome B-specific induced germination of Arabidopsis thaliana seeds. Seed Science Research 12, 253259.Google Scholar
Bethke, PC, Libourel, IG, Reinohl, V and Jones, RL (2006) Sodium nitroprusside, cyanide, nitrite, and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta 223, 805812.Google Scholar
Boudell, JA and Stromberg, JC (2015) Impact of nitrate enrichment on wetland and dryland seed germination and early seedling development. Journal of Vegetation Science 26, 452463.Google Scholar
Bouwmeester, HJ, Derks, L, Keizer, JJ and Karssen, CM (1994) Effects of endogenous nitrate content of Sisymbrium officinale seeds on germination and dormancy. Acta Botanica Neerlandica 43, 3950.Google Scholar
Bouwmeester, HJ and Karssen, CM (1993) Annual changes in dormancy and germination in seeds of Sisymbrium officinale (L.) Scop. New Phytologist 124, 179191.Google Scholar
Carrillo-Barral, N, Matilla, AJ, Iglesias-Fernández, R and Rodríguez-Gacio, MC (2013) Nitrate-induced early transcriptional changes during imbibition in non-after-ripened Sisymbrium officinale seeds. Physiologia Plantarum 148, 560573.Google Scholar
Carrillo-Barral, N, Matilla, AJ, Rodríguez-Gacio, MC and Iglesias-Fernández, R (2014) Nitrate affects sensu-stricto germination of after-ripened Sisymbrium officinale seeds by modifying expression of SoNCED5, SoCYP707A2 and SoGA3ox2 genes. Plant Science 217–218, 99108.Google Scholar
Carrillo-Barral, N, Matilla, AJ, García-Ramas, C and Rodríguez-Gacio, MC (2015) ABA-stimulated SoDOG1 expression is after-ripening inhibited during early imbibition of germinating Sisymbrium officinale seeds. Physiologia Plantarum 155, 457471.Google Scholar
Castaings, L, Camargo, A, Pocholle, D, Gaudon, V, Texier, Y, Boutet-Mercey, S, Taconnat, L, Renou, JP, Daniel-Vedele, F, Fernandez, E, Meyer, C and Krapp, A (2009) The nodule inception-like protein 7 modulations nitrate sensing and metabolism in Arabidopsis. The Plant Journal 57, 426435.Google Scholar
Chopin, F, Orsel, M, Dorbe, M-F, Chardon, F, Truong, H-N, Miller, AJ, Krapp, A and Daniel-Vedele, F (2007) The Arabidopsis ATNRT2.7 nitrate transporter controls nitrate content in seeds. Plant Cell 19, 15901602.Google Scholar
Deng, M, Moureaux, T and Caboche, M (1989). Tungstate, a molybdate analog inactivating nitrate reductase, deregulates the expression of the nitrate reductase structural gene. Plant Physiology 91, 304309.Google Scholar
Dong, T, Tong, J, Xiao, L, Cheng, H and Song, S (2012) Nitrate, abscisic acid and gibberellin interactions on the thermoinhibition of lettuce seed germination. Plant Growth Regulation 66, 191202.Google Scholar
Derkx, MPM and Karssen, CM (1993) Changing sensitivity to light and nitrate but not to gibberellins regulates seasonal dormancy patterns in Sisymbrium officinale seeds. Plant, Cell and Environment 16, 469479.Google Scholar
Finkelstein, RR and Lynch, TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12, 599609.Google Scholar
Finch-Savage, WE, Cadman, CSC, Toorop, PE, Lynn, JR and Hilhorst, HWM (2007) Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. The Plant Journal 51, 6078.Google Scholar
Finch-Savage, WE and Footitt, S (2012) To germinate or not to germinate: a question of dormancy relief not germination stimulation. Seed Science Research 22, 243248.Google Scholar
Finch-Savage, WE and Footitt, S (2017) Seed dormancy cycling and the regulation of dormancy mechanisms to time germination in variable field environments. Journal of Experimental Botany 68, 843856.Google Scholar
Footitt, S, Huang, Z, Clay, H, Mead, A and Finch-Savage, WE (2013) Temperature, light and nitrate sensing coordinate Arabidopsis seed dormancy cycling resulting in winter and summer annual phenotypes. The Plant Journal 74, 10031115.Google Scholar
Gibbs, DJ, Isa, NM, Movahedi, M, Lozano-Juste, J, Mendiondo, GM, Berckhan, S, Marín-de la Rosa, N, Conde, JV, Correia, CS, Pearce, SP, Bassel, GW, Hamali, B, Talloji, P, Tomé, DFA, Coego, A, Beynon, J, Alabadí, D, Bachmair, A, León, J, Gray, JE, Theodoulou, FL and Holdsworth, MJ (2014) Nitric oxide sensing in plants is mediated by proteolytic control of Group VII ERF transcription factors. Molecular Cell 53, 369379.Google Scholar
Grubisic, D and Konjevic, R (1990) Light and nitrate interaction in phytochrome-controlled germination of Paulownia tomentosa seeds. Planta 181, 239243.Google Scholar
Guan, P, Ripoll, J-J, Wang, R, Vuong, L, Bailey-Steinitz, J, Ye, D and Crawford, NM (2017) Interacting TCP and NLP transcription factors control plant responses to nitrate availability. Proceedings of the National Academy of Sciences USA 114, 24192424.Google Scholar
Gutiérrez, R. A., Gifford, ML, Poultney, C, Wang, R, Shasha, DE, Coruzzi, GM and Crawford, NM (2007) Insights into the genomic nitrate response using genetics and the Sungear Software System. Journal of Experimental Botany 58, 23592367.Google Scholar
He, H, Willems, LAJ, Batushansky, A, Fait, A, Hanson, J, Nijveen, H, Hilhorst, HWM and Bentsink, L (2015) Effects of parental temperature and nitrate on seed performance are reflected by partly overlapping genetic and metabolic pathways. Plant Cell Physiology 57, 473487.Google Scholar
He, H, Vidigal, DDS, Snoek, LB, Schnabel, S, Nijveen, H, Hilhorst, H and Bentsink, L (2014) Interaction between parental environment and genotype affects plant and seed performance in Arabidopsis. Journal of Experimental Botany 65, 66036615.Google Scholar
Hendricks, SB and Taylorson, RB (1972) Promotion of seed germination by nitrates and cyanides. Nature 237, 169170.Google Scholar
Hendricks, SB and Taylorson, RB (1974) Promotion of seed germination by nitrate, nitrite, hydroxyamine, and ammonium salts. Plant Physiology 54, 304309.Google Scholar
Hilhorst, HWM and Karssen, CM (1988) Dual effect of light on the gibberellin and nitrate-stimulated seed germination of Sisymbrium officinale and Arabidopsis thaliana. Plant Physiology 86, 591597.Google Scholar
Hilhorst, HWM and Karssen, CM (1989) Nitrate reductase independent stimulation of seed germination in Sisymbrium officinale L. (hedge mustard) by light and nitrate. Annals of Botany (Lond) 63, 131137.Google Scholar
Hilhorst, HWM, Smitt, CM and Karssen, CM (1986) Gibberellin-biosynthesis and -sensitivity mediated stimulation of seed germination of Sisymbrium officinale by red light and nitrate. Physiologia Plantarum 67, 267272.Google Scholar
Hilton, JR (1984) The influence of light and potassium nitrate on the dormancy and germination of Avena fatua L. (wild oat) seed and its ecological significance. New Phytologist 96, 3134.Google Scholar
Ho, CH, Lin, SH, Hu, HC and Tsay, YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138, 11841194.Google Scholar
Huang, Z, Olcer-Footitt, H, Footitt, S and Finch-Savage, WE (2015) Seed dormancy is a dynamic state: variable responses to pre- and post-shedding environmental signals in seeds of contrasting Arabidopsis ecotypes. Seed Science Research 25, 159169.Google Scholar
Huang, Z, Footitt, S, Tang, A and Finch-Savage, WE (2018) Predicted global warming scenarios impact on the mother plant to alter seed dormancy and germination behaviour in Arabidopsis. Plant, Cell and Environment 41, 187197.Google Scholar
Karssen, CM, Brinkhorst-van der Swan, DL, Breekland, AE and Koornneef, M (1983) Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh . Planta 157, 158165.Google Scholar
Kucera, B, Cohn, MA and Leubner-Metzger, G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15, 281307.Google Scholar
Kushiro, T, Okamoto, M, Nakabayashi, K, Yamagishi, K, Kitamura, S, Asami, T, Hirai, N, Koshiba, T, Kamiya, Y and Nambara, E (2004). The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. The EMBO Journal 23, 16471656.Google Scholar
Konishi, M and Yanagisawa, S (2010) Identification of a nitrate-responsive cis-element in the Arabidopsis NIR1 promoter defines the presence of multiple cis-regulatory elements for nitrogen response. The Plant Journal 63, 269282.Google Scholar
Konishi, M and Yanagisawa, S (2013) Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nature Communications 4, 1617.Google Scholar
Lee, KP, Piskurewicz, U, Tureckova, V, Strnad, M and Lopez-Molina, L (2010) A seed coat bedding assay shows that RGL2-dependent release of abscisic acid by the endosperm controls embryo growth in Arabidopsis dormant seeds. Proceedings of the National Academy of Sciences of the USA 107, 1910819113.Google Scholar
Lee, KP, Piskurewicz, U, Tureckova, V, Carat, S, Chappuis, R, Strnad, M, Fankhauser, C and Lopez-Molina, L (2012) Spatially and genetically distinct control of seed germination by phytochromes A and B. Genes and Development 26, 19841996.Google Scholar
Léran, S, Edel, KH, Pervent, M, Hashimoto, K, Corratgé-Faillie, C, Offenborn, JN, Tillard, P, Gojon, A, Kudka, J and Lacombe, B (2015) Nitrate sensing and uptake in Arabidopsis are enhanced by ABI2, a phosphatase inactivated by the stress hormone abscisic acid. Science Signaling 8, ra43. doi: 10.1126/scisignal.aaa4829Google Scholar
Leubner-Metzger, G (2003) Functions and regulation of b-1,3-glucanases during seed germination, dormancy release and after-ripening. Seed Science Research 13, 1734.Google Scholar
Liu, K-H and Tsay, Y-F (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. The EMBO Journal 22, 10051013.Google Scholar
Liu, KH, Niu, Y, Konishi, M, Wu, Y, Du, H, Chung, HS, Li, L, Boudsocq, M, McCormack, M, Maekawa, S, Ishida, T, Zhang, C, Shokat, K, Yanagisawa, S and Sheen, J (2017) Discovery of nitrate-CPK-NLP signalling in central nutrient-growth networks. Nature 545, 311316.Google Scholar
Liu, Y, Shi, L, Ye, N, Liu, R, Jia, W and Zhang, J (2009) Nitric oxide-induced rapid decrease of abscisic acid concentration is required in breaking seed dormancy in Arabidopsis. New Phytologist 183, 10301042.Google Scholar
Lopez-Molina, LL and Chau, N-H (2000). A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thaliana. Plant Cell Physiology 41, 541547.Google Scholar
Luna, B and Moreno, JM (2009) Light and nitrate effects on seed germination of Mediterranean plant species of several functional groups. Plant Ecology 203, 123135.Google Scholar
Matakiadis, T, Alboresi, A, Jukumaru, Y, Tatematsu, K, Pichon, O, Renou, J-P, Kamiya, Y, Nambara, E and Truong, H-N (2009) The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiology 149, 949960.Google Scholar
Marchive, C, Roudier, F, Castaings, L, Bréhaut, V, Blondet, E, Colot, V, Meyer, C and Krapp, A (2013) Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nature Communications 4, 1713.Google Scholar
Nambara, E, Okamoto, M, Tatematsu, K, Yano, R, Seo, M and Kamiya, Y (2010) Abscisic acid and the control of seed dormancy and germination. Seed Science Research 20, 5567.Google Scholar
Ogawa, M, Hanada, A, Yamauchi, Y, Kuwahara, A, Kamiya, Y and Yamaguchi, S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15, 15911604.Google Scholar
Okamoto, M, Kuwahara, A, Seo, M, Kushiro, T, Asami, T, Hirai, N, Kamiya, Y, Koshiba, T and Nambara, E (2006) CYP707A1 and CYP707A2, which encode ABA 8′-hydroxylases, are indispensable for a proper control of seed dormancy and germination in Arabidopsis. Plant Physiology 141, 97107.Google Scholar
Penfield, S (2017) Seed dormancy and germination. Current Biology 27, R874878.Google Scholar
Pill, WG, Frett, JJ and Morneau, DC (1991) Germination and seedling emergence of primed tomato and asparagus seeds under adverse conditions. HortScience 26, 11601162.Google Scholar
Ponert, J, Figura, T, Vosolsobe, S, Lipavská, H, Vohník, M and Jersáková, J (2015) Asymbiotic germination of mature seeds and protocorm development of Pseudorchis albida (Orchidaceae) are inhibited by nitrates even at extremely low concentrations. Botany 91, 662670.Google Scholar
Pons, TL (1989) Breaking of seed dormancy by nitrate as a gap detection mechanism. Annals of Botany 63, 139143.Google Scholar
Preston, J, Tatematsu, K, Kanno, Y, Hobo, T, Kimura, M, Jikumaru, Y, Yano, R, Kamiya, Y and Nambara, E (2009) Temporal expression patterns of hormone metabolism genes during imbibition of Arabidopsis thaliana seeds: a comparative study on dormant and non-dormant accessions. Plant Cell Physiology 50, 17861800.Google Scholar
Redinbaugh, MG and Campbell, WH (1993) Glutamine synthetase and ferredoxin-dependent glutamate synthase expression in the maize (Zea mays) root primary response to nitrate (evidence for an organ-specific response). Plant Physiology 101, 12491255.Google Scholar
Riveras, E, Alvarez, JM, Vidal, EA, Oses, C, Vega, A and Gutierrez, RA (2015) The calcium ion is a second messenger in the nitrate signaling pathway of Arabidopsis. Plant Physiology 169, 13971404.Google Scholar
Saini, HS, Bassi, PK and Spencer, MS (1985). Seed germination in Chenopodium album L.: relationships between nitrate and the effects of plant hormones. Plant Physiology 77, 940943.Google Scholar
Scheible, WR, Morcuende, R, Czechowski, T, Fritz, C, Osuna, D, Palacios-Rojas, N, Schindelasch, D, Thimm, O, Udvardi, MK and Stitt, M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiology 136, 24832499.Google Scholar
Seo, M, Nambara, E, Choi, G and Yamaguchi, S (2009) Interaction of light and hormone signals in germinating seeds. Plant Molecular Biology 69, 463472.Google Scholar
Shim, SI, Moon, J-C, Jang, CS, Raymer, P and Kim, W (2008) Effect of potassium nitrate priming on seed germination of seashore Paspalum. HortScience 43, 22592262.Google Scholar
Toole, EH, Toole, VK, Borthwick, HA and Hendricks, SB (1955) Photocontrol of Lepidium seed germination. Plant Physiology 30, 1521.Google Scholar
Toorop, PE (2015) Nitrate controls testa rupture and water content during release of physiological dormancy in seeds of Sisymbrium officinale (L.) Scop. Seed Science Research 25, 138146.Google Scholar
Topham, AT, Taylor, RE, Yan, D, Nambara, E, Johnston, IG and Bassel, GW (2017) Temperature variability is integrated by a spatially embedded decision-making center to break dormancy in Arabidopsis seeds. Proceedings of the National Academy of Sciences of the USA 114, 66296634.Google Scholar
Toyomasu, T, Tsuji, H, Yamane, H, Nakayama, M, Yamaguchi, I, Murofushi, N, Takahashi, N and Inoue, Y (1993) Light effects on endogenous levels of gibberellins in photoblastic lettuce seeds. Journal of Plant Growth Regulation 12, 8590.Google Scholar
Thompson, K and Ooi, MKJ (2010) To germinate or not to germinate: more than just a question of dormancy. Seed Science Research 20, 209211.Google Scholar
Tsay, YF, Chiu, CC, Tsai, CB, Ho, CH and Hsu, PK (2007) Nitrate transporters and peptide transporters. FEBS Letters 581, 22902300.Google Scholar
Wang, M, van der Meulen, R, Visser, K, van Schaik, H-P, van Duijn, B and de Boer, AH (1998) Effects of dormancy-breaking chemicals on ABA levels in barley grain embryos. Seed Science Research 8, 129137.Google Scholar
Wang, R, Okamoto, M, Xing, X and Crawford, NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiology 132, 556567.Google Scholar
Wang, R, Tischner, R, Gutiérrez, RA, Hoffman, M, Xing, X, Chen, M, Coruzzi, G and Crawford, NM (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiology 136, 25122522.Google Scholar
Wang, R, Xing, X and Crawford, N (2007) Nitrate acts as a transcriptome signal at micromolar concentrations in Arabidopsis roots. Plant Physiology 145, 17351745.Google Scholar
Wang, R, Xing, X, Wang, Y, Tran, A and Crawford, NM (2009) A genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1.1. Plant Physiology 151, 472478.Google Scholar
Yamaguchi, S (2008) Gibberellin metabolism and its regulation. Annual Review of Plant Biology 59, 225251.Google Scholar
Yan, D, Easwaran, V, Chau, V, Okamoto, M, Ierullo, M, Kimura, M, Endo, A, Yano, R, Pasha, A, Gong, Y, Bi, YM, Provart, N, Guttman, D, Krapp, A, Rothstein, SJ and Nambara, E (2016) NIN-like protein 8 is a master regulator of nitrate-promoted seed germination in Arabidopsis. Nature Communications 7, 13179. doi: 10.1038/ncomms13179Google Scholar
Yan, D, Duermeyer, L, Leoveanu, C and Nambara, E (2014) The functions of the endosperm during germination. Plant Cell Physiology 55, 15211533.Google Scholar